A BMP7 variant inhibits the tumorigenic potential of glioblastoma stem-like cells

Cell Death and Differentiation

Volumn 19, Issue 10, 2012, Pages 1644-1654

  Tate, C M ^a   Pallini, R ^b   Ricci Vitiani, L ^c   Dowless, M ^a   Shiyanova, T ^a   D'Alessandris, G Q ^b   Morgante, L ^b   Giannetti, S ^b   Larocca, L M ^b   Di Martino, S ^c   Rowlinson, S W ^a   De Maria, R ^c   Stancato, L ^a  

^a ELI LILLY AND COMPANY   (United States)

^b CATHOLIC UNIVERSITY   (Italy)

^c ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

bone morphogenetic protein; cancer stem cells; Glioblastoma

Indexed keywords

BETA TUBULIN; BETA3 TUBULIN; GLIAL FIBRILLARY ACIDIC PROTEIN; NESTIN; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; OSTEOGENIC PROTEIN 1; PROTEIN VARIANT; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; ASTROCYTE; CANCER CONTROL; CANCER GROWTH; CANCER INHIBITION; CANCER INVASION; CANCER MODEL; CANCER MORTALITY; CANCER STEM CELL; CANCER SURVIVAL; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM; GLIOBLASTOMA; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR XENOGRAFT;

ANIMALS; BONE MORPHOGENETIC PROTEIN 7; BRAIN NEOPLASMS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; CYTOKINES; GLIOBLASTOMA; HCT116 CELLS; HUMANS; MICE; NEOPLASTIC STEM CELLS; NEOVASCULARIZATION, PATHOLOGIC; TRANSPLANTATION, HETEROLOGOUS;

MUS;

EID: 84866116474     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2012.44     Document Type: Article

References (40)

1. Furnari F, Fenton T, Bachoo R, Mukasa A, Stommel J, Stegh A et al. Malignant astrocytic glioma: genetics, biology and paths to treatment. Genes Dev 2007; 21: 2683-2710. (Pubitemid 350070717)
2. Butowski N, Chang S. Glial tumors: the current state of scientific knowledge Clin Neurosurg 2006; 53: 106-113.
3. Eramo A, Ricci-Vitiani L, Zeuner A, Pallini R, Lotti F, Sette G et al. Chemotherapy resistance of glioblastoma stem cells. Cell Death Diff 2006; 13: 1238-1241. (Pubitemid 43905604)
4. Singh S, Clarke I, Terasaki M. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003; 63: 5821-5828. (Pubitemid 37187480)
5. Vescovi A, Galli R, Reynolds B. Brain tumour stem cells. Nat Rev 2006; 6: 425-435.
6. Huang Z, Cheng L, Guryanova O, Wu Q, Bao S. Cancer stem cells in glioblastoma-molecular signaling and therapeutic targeting. Protein Cell 2010; 1: 638-655.
7. Rich J, Bao S. Chemotherapy and cancer stem cells. Cell Stem Cell 2007; 1: 353-355. (Pubitemid 47506543)
8. Bao S, Wu Q, Sathornsumetee S, Hao Y, Li Z, Hjelmeland A et al. Stem cell-like glioma cells promote tumor angiogenesis through vascular endothlial growth factor. Cancer Res 2006; 66: 7843-7848. (Pubitemid 44299144)
9. Ricci-Vitiani L, Pallini R, Biffoni M, Todaro M, Invernici G, Cenci T et al. Tumour vascularization via endothelial differntiation of glioblastoma stem-like cells. Nature 2010; 468: 824-828.
10. Wang R, Chadalavada K, Wilshire J, Kowalik U, Hovinga K, Geber A et al. Glioblastoma stem-like cells give rise to tumour endothelium. Nature 2010; 468: 829-833.
11. Lee J, Jin Son M, Woolard K, Donin N, Li A, Cheng C-H et al. Epigenetic-mediated dysfunction of the bone morphogenetic protein developmental pathway inhibits differentiation of human glioblastoma tumor initiating cells. Cancer Cell 2008; 13: 69-80. (Pubitemid 350309742)
12. Gross R, Mehler M, Mabie P, Zang Z, Santschi L, Kessler J. Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron 1996; 17: 595-606. (Pubitemid 26365340)
13. Anderson G, Darshan D. Small-molecule dissection of BMP signaling. Nature Chemical Biology 2008; 4: 15-16. (Pubitemid 350273659)
14. Pallini R, Ricci-Vitiani L, Banna G, Signore M, Lombardi D, Todaro M et al. Cancer stem cell analysis and clinical outcome in patients with glioblastoma multiforme. Clin Cancer Res 2008; 14: 8205-7212.
15. Low J, Dowless M, Shiyanova T, Rowlinson S, Ricci-Vitiani L, De Maria R et al. Knockdown of cancer testis antigens modulates neural stem cell marker expression in glioblastoma tumor stem cells. J Biomol Screen 2010; 15: 830-839.
16. Annovazzi L, Mellai M. Caldera V, Valente G, Schiffer D. SOX2 expression and amplification in gliomas and glioma cell lines. Cancer Genom Proteom 2011; 8: 139-147.
17. Po A, Ferretti E, Miele E, De Smaele E, Paganelli A, Canettieri G et al. Hedgehog controls neural stem cells through p53-independent regulation of Nanog. EMBO J 2010; 29: 2646-2658.
18. Bao S, Wu Q, Li Z, Sathornsumetee S, Wang H, McLendon R et al. Targeting cancer stem cells through L1CAM suppresses glioma growth. Cancer Res 2008; 68: 6043-6048.
19. Holland E. Progenitor cells and glioma formation. Curr Opin Neurol 2001; 14: 683-688. (Pubitemid 34060103)
20. Duggal N, Hammond R. Nestin expression in ganglioglioma. Exp Neurol 2002; 174: 89-95. (Pubitemid 34218912)
21. Lamszus K, Gunther H. Glioma stem cells as a target for treatment. Target Oncol 2010; 5: 211-215.
22. Ricci-Vitiani L, Pallini R, Larocca L, Lombadi D, Signore M, Pierconti F et al. Mesenchymal differentiation of glioblastoma stem cells. Cell Death Diff 2008; 15: 1491-1498.
23. Low J, Huang S, Blosser W, Dowless M, Burch J, Neubauer B et al. High content imaging characterization of cell cycle therapeutics through in vitro and in vivo subpopulation analysis. Mol Cancer Ther 2008; 7: 2455-2463.
24. Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S et al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 2004; 64: 7011-7021. (Pubitemid 39331011)
25. Piccirillo S, Binda E, Fiocco R, Vescovi A, Shah K. Brain cancer stem cells. J Mol Med 2009; 87: 1087-1095.
26. Li Z, Bao S, Wu Q, Wang H, Eyler C, Sathornsumetee S et al. Hypoxia inducible factors regulate tumorigenic capacity of glioma stem cells. Cancer Cell 2009; 15: 501-513.
27. Hogan B. Bone morphogenetic proteins in development. Curr Opin Genet Dev 1996; 6: 432-438. (Pubitemid 26280795)
28. Cavallaro M, Mariani J, Lancini C, Latorre E, Caccia R, Gullo F et al. Impaired generation of mature neurons by neural stem cells from hypomorphic Sox2 mutants. Development 2008; 135: 541-557.
29. Ferri A, Cavallaro M, Braida D, Cristofano A, Canta A, Vezzani A et al. Sox2 deficiency causes neurdegeneration and impaired neurogenesis in the adult mouse brain. Development 2004; 131: 3805-3819. (Pubitemid 39199387)
30. Strojnik T, Rosland G, Sakariassen P, Kavalar R, Lah T. Neural stem cell markers, nestin and musashi proteins, in the progression of human glioma: correlation of nestin with prognosis of patient survival. Surg Neurol 2007; 68: 133-143. (Pubitemid 47087905)
31. Gangemi R, Griffero F, Marubbi D, Perera M, Capra M, Malatesta P et al. SOX2 silencing in glioblastoma tumor-initiating cells causes stop of proliferation and loss of tumorigenicity. Stem Cells 2009; 27: 40-48.
32. Ligon K, Huilard E, Mehta S, Kesari S, Liu H, Alberta J et al. Olig2-regulated lineage-restricted pathway controls replication competence in neural stem cells and malignant glioma. Neuron 2007; 53: 503-517. (Pubitemid 46216748)
33. Chirasani S, Sternjak A, Wend P, Momma S, Campos B, Herrmann I et al. Bone morphogenetic protein-7 release from endogenous neural precursor cells suppresses the tumourigenicity of stem-like glioblastoma cells. Brain 2010; 133: 1961-1972.
34. Lombardo Y, Scopelliti A, Cammareri P, Todaro M, Iovino F, Ricci-Vitiani L et al. Bone morphogenetic protein 4 induces differentiation of colorectal cancer stem cells and increases their response to chemotherapy in mice. Gastroenterology 2011; 140: 297-309.
35. Piccirillo S, Reynolds B, Zanetti N, Lamorte G, Binda E, Broggi G et al. Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 2006; 444: 761-765. (Pubitemid 44949605)
36. Jain R, di Tomaso E, Duda D, Loeffler J, Sorensen A, Batchelor T. Angiogenesis in brain tumours. Nature 2007; 8: 610-622. (Pubitemid 47093931)
37. Swencki-Underwood B, Mills J, Vennarini J, Boakye K, Luo J, Pomerantz S. Expression and characterization of a human BMP-7 variant with improved biochemical properties. Protein Expr Purif 2008; 57: 312-319. (Pubitemid 350296967)
38. Low J, Shuguang H, Dowless M, Blosser W, Vincent T, Davis S et al. High-content imaging analysis of the knockdown effects of validated siRNAs and antisense oligonucleotides J Biomol Screen 2007; 12: 776-788.
39. Pallini R, Sorrentino A, Pierconti F, Maggiano N, Faggi R, Montano M et al. Telomerase inhibition by stable RNA interference impairs tumor growth and angiogenesis in glioblastoma xenografts. Int J Cancer 2006; 118: 2158-2167.
40. Mollinari C, Ricci-Vitiani L, Pieri M, Lucantoni C, Rinaldi A, Racaniello M et al. Downregulation of thymosin beta 4 in neural progenitor grafts promotes spinal cord regeneration. J Cell Sci 2009; 122: 4195-4207.